Associations of reading skills and properties of cerebral white matter pathways in 8-year-old children born preterm

AIM: Children born preterm (PT) experience perinatal white matter injury and later reading deficits at school age. We used two complementary neuroimaging modalities to determine if reading skills would be associated with contemporaneous white matter properties in school-aged PT children. METHOD: In 8-year-old PT children (N=29), we measured diffusivity (fractional anisotropy, FA), from diffusion MRI, and myelin content (relaxation rate, R1) from quantitative relaxometry. We assessed reading (Gray's Oral Reading Test, Fifth Edition) in each child. Whole-brain deterministic tractography coupled with automatic segmentation and quantification were applied to extract FA and R1 along four tracts and assess their statistical association with reading scores. RESULTS: Reading-FA correlations were not significant along the four analyzed tracts. Reading-R1 correlations were significantly positive in portions of the left superior longitudinal fasciculus, right uncinate fasciculus, and left inferior longitudinal fasciculus. FA positively correlated with R1 in limited areas of reading-R1 associations, but did not contribute to the variance in reading scores. INTERPRETATION: Combining complementary neuroimaging approaches identified relations between reading and white matter properties not found using a single MRI measure. Associations of reading skills and white matter properties may vary across white matter tracts and metrics in PT children.

[1]  H. Feldman,et al.  Associations of Reading Efficiency with White Matter Properties of the Cerebellar Peduncles in Children , 2020, The Cerebellum.

[2]  C. Lebel,et al.  Multimodal principal component analysis to identify major features of white matter structure and links to reading , 2020, bioRxiv.

[3]  Shir Filo,et al.  Disentangling molecular alterations from water-content changes in the aging human brain using quantitative MRI , 2019, Nature Communications.

[4]  V. Marchman,et al.  White Matter Plasticity in Reading-Related Pathways Differs in Children Born Preterm and at Term: A Longitudinal Analysis , 2019, Front. Hum. Neurosci..

[5]  H. Feldman,et al.  More than myelin: Probing white matter differences in prematurity with quantitative T1 and diffusion MRI , 2019, NeuroImage: Clinical.

[6]  V. Marchman,et al.  White matter properties associated with pre‐reading skills in 6‐year‐old children born preterm and at term , 2018, Developmental medicine and child neurology.

[7]  D. Wechsler Wechsler Abbreviated Scale of Intelligence--Second Edition , 2018 .

[8]  Paulina A. Kulesz,et al.  White matter microstructure integrity in relation to reading proficiency☆ , 2017, Brain and Language.

[9]  S. Back White matter injury in the preterm infant: pathology and mechanisms , 2017, Acta Neuropathologica.

[10]  H. Feldman,et al.  White matter properties differ in 6-year old Readers and Pre-readers , 2017, Brain Structure and Function.

[11]  H. Feldman,et al.  White matter properties differ in 6-year old Readers and Pre-readers , 2016, Brain Structure and Function.

[12]  N. Gaab,et al.  Development of Tract‐Specific White Matter Pathways During Early Reading Development in At‐Risk Children and Typical Controls , 2016, Cerebral cortex.

[13]  N. Myall,et al.  Variations in the neurobiology of reading in children and adolescents born full term and preterm , 2016, NeuroImage: Clinical.

[14]  A. Lutti,et al.  Advances in MRI-based computational neuroanatomy: from morphometry to in-vivo histology. , 2015, Current opinion in neurology.

[15]  H. Feldman,et al.  Reading abilities in school‐aged preterm children: a review and meta‐analysis , 2015, Developmental medicine and child neurology.

[16]  B. Wandell,et al.  Lifespan maturation and degeneration of human brain white matter , 2014, Nature Communications.

[17]  Robert Turner,et al.  Myelin and iron concentration in the human brain: A quantitative study of MRI contrast , 2014, NeuroImage.

[18]  Derek K. Jones,et al.  Why diffusion tensor MRI does well only some of the time: Variance and covariance of white matter tissue microstructure attributes in the living human brain☆ , 2014, NeuroImage.

[19]  Gary F. Egan,et al.  Regional white matter microstructure in very preterm infants: Predictors and 7 year outcomes , 2014, Cortex.

[20]  Derek K. Jones,et al.  Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging , 2013, Human brain mapping.

[21]  Daniel Rueckert,et al.  The influence of preterm birth on the developing thalamocortical connectome , 2013, Cortex.

[22]  Josef Parvizi,et al.  Quantifying the local tissue volume and composition in individual brains with MRI , 2013, Nature Medicine.

[23]  Anna H. Hall,et al.  Test Review: J. L. Wiederholt & B. R. Bryant. (2012). Gray Oral Reading Tests—Fifth Edition (GORT-5). Austin, TX: Pro-Ed. , 2013 .

[24]  B. Wandell,et al.  Development of white matter and reading skills , 2012, Proceedings of the National Academy of Sciences.

[25]  Daniel C. Alexander,et al.  NODDI: Practical in vivo neurite orientation dispersion and density imaging of the human brain , 2012, NeuroImage.

[26]  J. Wouters,et al.  Neuroscience and Biobehavioral Reviews a Qualitative and Quantitative Review of Diffusion Tensor Imaging Studies in Reading and Dyslexia , 2022 .

[27]  Michelle Hampson,et al.  Microstructural and functional connectivity in the developing preterm brain. , 2011, Seminars in perinatology.

[28]  Gro C. Christensen Løhaugen,et al.  Young adults born preterm with very low birth weight demonstrate widespread white matter alterations on brain DTI , 2011, NeuroImage.

[29]  Brian A. Wandell,et al.  Bound pool fractions complement diffusion measures to describe white matter micro and macrostructure , 2011, NeuroImage.

[30]  B. Luna,et al.  Reading performance correlates with white‐matter properties in preterm and term children , 2010, Developmental medicine and child neurology.

[31]  Emily A. Farris,et al.  Brain connectivity in non-reading impaired children and children diagnosed with developmental dyslexia , 2009, Neuropsychologia.

[32]  Volkmar Glauche,et al.  Ventral and dorsal pathways for language , 2008, Proceedings of the National Academy of Sciences.

[33]  P. Basser,et al.  Axcaliber: A method for measuring axon diameter distribution from diffusion MRI , 2008, Magnetic resonance in medicine.

[34]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[35]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. 1996. , 1996, Journal of magnetic resonance.

[36]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[37]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. , 1996, Journal of magnetic resonance. Series B.

[38]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[39]  N J Pelc,et al.  Rapid calculation of T1 using variable flip angle gradient refocused imaging. , 1987, Magnetic resonance imaging.

[40]  A. B. Hollingshead,et al.  Four factor index of social status , 1975 .